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Abstract

Background

As the various systems in the body are inter-connected to form a single structural
unit, a pathological condition in one area can also affect other areas. There are
many known correlations between the visual and motor system. The importance of visual
function, particularly the paracentral peripheral field of view, in motor coordination,
ambulation and the maintenance of balance has been amply demonstrated.

In line with current medical principles, which are moving towards a more holistic
view of the human body, this study aims to investigate, in an interdisciplinary manner,
the incidence of dental malocclusions together with posture and eye convergence disorders.

Methods

Six hundred and five children attending at the 3rd, 4th and 5th years of seven Genoa primary schools were examined. Each child underwent the following
examinations: (i) dental/occlusal; (ii) orthoptic; and (iii) postural. Occlusal data
concerned the presence of cross-bite, midline deviation with a mandibular shift, bad
habits and deep or open bite.

Postural assessment involved frontal and lateral inspection, investigation during
trunk flexion and ambulation, and note of any asymmetry in the lower limbs. The recorded
orthoptic data included those pertaining to ocular dominance, a cover test, convergence
and the Brock string test.

Results

A prevalence of cases with an unphysiological gait was found in patients with overjet
(14.70%) or overbite (14.87%), while the percentage of patients with normal occlusion
that showed an unphysiological gait was 13.08%. Also, about 93.8%–94.2% of children
showed normal legs without dysmetry, with no difference in respect to the type of
occlusion. Subjects with an open bite or deep bite showed a slightly different distribution
of right or left dominant eyes.

Conclusion

About 13% of children showed a pathological gait and, among them, vertical anomalies
of occlusion (deep bite or open bite) were prevalent with respect to the other occlusal
defects. The vertical dimension of occlusion revealed a slight relationship with the
proper dominant eye. Postural, orthoptic, osteopathic and occlusal variables were
often clinically associated, and therefore these disorders appear to request a multidisciplinary
medical approach for their treatment.

Keywords:

Teeth malocclusions; Wrong posture; Ocular convergence disorders

Background

As the various systems in the body are inter-connected to form a single structural
unit, a pathological condition in one area can also affect other areas. In particular,
the skeletal muscles play a decisive role in the coincidence of various disorders,
because of the continuous anatomical and functional “chain” they form between the
skull, lower jaw, spine, limbs and pelvis [1-5].

Indeed, if a situation of muscular high tension arises in one of the links in this
chain (mandible, hyoid, vertebrae, pelvis and limbs), it is immediately transmitted
to the rest of the body. As a consequence, the body loses its state of equilibrium,
giving rise to compensation mechanisms, for example muscular tension in other antagonistic
parts of the body. In this way, dental malocclusion can be associated with misalignment
of the mandible, one of the links in the muscular chain, leading to hyper-contraction
of the masticatory muscles [6]. This tension forces the rest of the body to react, imposing postural modifications
brought about by the contraction of other muscles in the chain. In fact, the incidence
of malocclusion in orthopedic patients reported in the literature ranges from 83%
to 87% [7]. Furthermore, it is now widely recognized that problems involving the stomatognathic
apparatus and alterations in feet posture can cause kinetic dysfunction, leading to
pathologies in the ascending and descending spinal tracts [7,8].

Moreover, it has become increasingly evident that disorders of the sensory nervous
system can have a considerable influence on regulation of motor function [8]. In fact, modifications in these sensory neurons can cause parafunctional alterations
and pathologies in apparently unrelated body districts, For instance, dental malocclusion
can cause pain elsewhere in the body. Because of its position, misalignment of the
mandible can also cause the position of the pupillary line to be momentarily altered,
provoking the intervention of ocular muscles to keep the gaze straight.

There are many known correlations between the visual and motor systems, and the importance
of visual function, particularly the paracentral peripheral field of view, in motor
coordination, ambulation and the maintenance of balance has been amply demonstrated
[10]. In fact, to follow an object in motion, the eye needs to be able to coordinate the
movement of the head and neck. The musculature controlling eye movement is closely
connected to the stomatognathic system. Fibers emerging from the muscle spindles and
palisade endings in the oculomotor muscles, especially the lateral rectus muscle,
form pathways to the oculomotor nuclei and the trigeminal nucleus [11-13]. Ocular defects that can be linked to dental malocclusion are convergence defects,
heterophoria, heterotrophia and esodeviations.

This study is based on three presuppositions: 1) a mandibular shift may cause a positional
head adaptation [13]; 2) ocular phorias may cause a head compensation posture called ocular torticollis
[14]; and 3) a head compensation posture causes body adaptation positions, to maintain
a center of gravity compatible with the upright position [15]. Head positions enhance postural compensation phenomena; thereby head position is
a key point in body balance. This is demonstrated by the great incidence of cervical
pain due to muscular tension, which means head posture controls hyperfunctions [16,17].

In this study, the aim was to determine if these disorders occur with significant
frequency in children (aged 7–10 years). We analyzed in primis dental malocclusions (by an orthodontist) and subsequently orthophoria was recorded
(by an orthoptist). Then the cranio-sacral respiratory rhythm was tested (by an osteopath).
The incidence and concomitant frequency of these disorders were statistically analyzed
to understand whether a causal connection existed in situations where patients were
forced to carry out functional compensations in different body districts.

Methods

In this epidemiological study, conducted with the collaboration of the local health
authority (ASL 3, 1st District, School Medicine Services), 605 children (mean age 8.5 ± 2.3 years; 45%
males; 55% females) attending the 3rd, 4th and 5th years of seven Genoa primary schools were examined.

Before any clinical research was performed, the parents of the children attending
the selected classes were asked to provide informed consent and to fill in an anamnestic
survey (i.e., birth, breast and/or formula feeding habits, dummy- or thumb-sucking,
headaches, dental and general trauma, pain in the muscles of the head and neck and
nocturnal bruxism). The questionnaire pertaining to each child was then used at subsequent
clinical examinations to notify the medical specialists of any related disorders,
thereby assisting them in the formation of an accurate clinical picture. During this
screening, each child underwent the following examinations: 1) dental/occlusal; 2)
orthoptic; and 3) osteopathic-postural. These investigations were performed at the
school by two dentists, one orthoptist and one osteopathist, under the expert supervision
of a clinician specialized in School Medicine (from the ASL 3, 1st District). The examination protocol adopted was based on previous studies [16,17].

Three clinical evaluation forms that were previously designed were used to record
the dental, orthoptic and postural data, and a medical record of each child was compiled.

Postural assessment involved frontal and lateral inspection, investigation during
trunk flexion and ambulation, and note of any asymmetry in the lower limbs was taken
(Figure 1). The collected dental information contained details of the molar and canine relationships,
dental and facial midline, overbite, transversal relationships (cross-bite presence/absence),
bad habits, hygiene and ongoing orthodontic treatment (Figure 2). The recorded orthoptic data included those pertaining to a cover test, convergence,
ocular dominance and the Brock string test (Figures 3, 4, 5).

Figure 1.Postural assessment involved frontal and lateral inspection, investigation during
trunk flexion and ambulation, and note of any asymmetry in the lower limbs or shoulders
was taken.

The following eye tests were carried out primarily to determine postural information:

Cover/uncover test (CT; Figure 3): The test was performed by covering and uncovering each eye in turn (e.g., with
a hand or occluder) while the patient fixated on a small object. The purpose of the
test was to determine any re-fixation movement in the uncovered eye. In this way,
each eye was considered as a single entity and any axial defects (heterophoria) were
detected by the presence of re-fixation movements in the uncovered eye (dissociation
of the right and left eyes). An experienced ophthalmologist was then able to quantify
the degree of phoria by passing a test card featuring increasing prism diopter values
before the eyes until the re-fixation movement disappeared.

Convergence test (CT; Figure 4): The test was performed up to the base of the nose to determine the degree of tonic
(dynamic), fusional and accommodative convergence.

There are two types of convergence:

Dynamic convergence (smooth pursuit system), which is considered pathological if the
saccadic movements of one eye are slower than the other, the convergence movement
of one or both eyes fails to complete, or the eye or eyes wander outwards when attempting
to converge. Postural imbalance resulting from this condition will be greater if the
defect is more pronounced in one eye.

Reflexive convergence (saccadic system), which seems to involve the saccadic rather
than pursuit system, and is considered pathological if an eye fails to converge, stops
in transit or wanders outwards when attempting to perform convergence. If the two
eyes contradict each other, the convergence defect is considered to be present in
both eyes. If the hypoconvergent eye protrudes and points downwards during reflexive
convergence, a phoria or trophia is likely to be present.

Ocular dominance test (Figure 5): A card with a hole of diameter 2 cm is placed a distance of 10–15 cm from the patient’s
eyes. The patient is then asked to stare through the hole at a distant object and
the eye that automatically complies is the dominant eye. Confirmation of ocular dominance
can be achieved by covering each eye in turn and repeating the test. Without moving
the pierced card, the dominant eye will be the only one able to see the object in
the center of the hole.

Parents were present and fully informed about the clinical findings. All patients
approved the inclusion of their data in this study. The research reported in the paper
was undertaken in compliance with the Helsinki Declaration. Ethical approval was granted
by the Ethics Committee of the S. Martino Hospital- University of Genoa-National Institute
for Cancer Research (P.R 21/12). Written consent was obtained after orientation to
the study.

Statistical evaluation

All data were analyzed in the form of percentages of subjects with a particular occlusal
or postural or ocular situation. The percentages of subjects with postural or ocular
diseases were compared among subjects with a normal, deep or open bite.

A chi-square test was used to evaluate the null hypothesis stating that the frequency
distributions of gait posture, leg dysmetry or ocular diseases observed in our sample
were consistent with a particular theoretical distribution. The null hypothesis was
that the considered diseases were mutually exclusive and had the same probability
for each type of teeth bite (open, normal or deep bite) because all the disease outcomes
were equally likely to occur. The percentages were compared with a chi-square test.
The p level was set at 0.05.

The software SPSS 9.0 was employed to evaluate statistical tests.

Results

A total of 605 children students (mean age 8.5 ± 2.3 years; 45% males; 55% females)
were examined.

Table 1.Distribution of physiological and pathological gait in our population

There was a prevalence of cases with an unphysiological gait in patients with an abnormal
overjet (14.7%) or overbite (14.87%), while the percentage of patients with normal
occlusion that showed an unphysiological gait was 13.08%.

In our sample, about 85.3%–86.9% of the subjects showed a physiological gait.

Table 2 shows the results for dysmetric legs. In our sample, the percentages of subjects
with dysmetric legs were lower than the percentages of subjects with a pathological
gait, suggesting that about 5%–7% of the cases with a pathological gait were due to
other factors (Table 2). Also, about 93.85%–94.2% of the children had normal legs, without respect to the
type of teeth bite (Table 2).

Table 3 shows the data for the ocular dominant test. The majority of subjects had a right
dominant eye (386 subjects vs. 221 subjects), which means 63%–67% had a right dominant
eye and 33%–37% of the subjects had a left dominant eye. Subjects with an open bite
showed a slightly different distribution with a lower difference between the percentages
of right or left dominant eyes. In the ocular dominance test (Table 3), patients with an open bite with a right dominant eye vs. left dominant eye were
58.42% and 41.58%, respectively. Patients with a deep bite that showed a right dominant
eye were 66.66% while 33.33% had a left dominant eye. Patients with normal occlusion
with a right dominant eye were 62.7% and those with a left dominant eye were 37.3%.

Subjects with an open bite showed a significantly lower percentage (2.97%) of CT-eso
with respect to subjects with a normal bite or deep bite. Subjects with a deep bite
showed a significantly higher percentage of CT-exo with respect to subjects with a
normal or open bite.

Table 5 shows the data for ocular convergence (normal, pathological on the right side or
pathological on the left side). Patients with an open bite showed a significantly
higher prevalence (8.65%) of pathological convergence in the left eye with respect
to subjects with a normal or deep bite. Patients with a deep bite showed a significantly
lower percentage (3.70%) of pathological convergence in the right eye with respect
to the other groups.

Discussion

The dominant eye

A difference was noted in the observed percentages in the open bite children that
showed a left dominant eye (41.58%), which was higher than children with a deep bite
or normal bite. Deep bite subjects were more likely to show a right dominant eye (66.6%)
with respect to children with a normal bite or open bite. The data suggested that
the tendency of the vertical dimension of the bite (deep bite or open bite) was related
to the dominant eye. The relationship between the dominant eye and the mandibular
position was reported in terms of change in the transverse plane of the head posture
after positioning eye patches over the dominant eye for 1 h [18].

Ocular convergence disorders (phorias)

Subjects with an open bite showed a significantly lower percentage (2.97%) of CT-esophoria
with respect to subjects with a normal bite or deep bite. As in other forms of strabismus,
esodeviation can be controlled by fusional divergence (esophoria), intermittently
controlled by fusional divergence (intermittent esotrophia) or constantly manifest
(esotrophia). Subjects with a deep bite showed a significantly higher percentage of
CT-exophoria with respect to subjects with a normal or open bite.

Other studies have shown the relationships of dental occlusion, the oculomotor system
and visual stabilization. Evidence for a correlation between eyes and dental occlusion
came from the use of mandibular orthopedic repositioning appliances, which simultaneously
modify mandibular position and visual focusing tests using prismatic bars. These phenomena
gradually disappear after removal of the appliance.

Associations also exist between TMD and oculomotor function. Some authors suggested
a much higher prevalence of ocular convergence defects in TMD adults presenting with
a limited maximal opening, myofascial pain and pain in the neck and shoulder area
[18].

Numerous anatomical connections have been described between trigeminal systems and
the nervous structures involved in maintaining posture. The mesencephalic nucleus
of the trigeminus, which extends itself from the dorsal portion of the spinal trigeminal
nucleus to the caudal part of the superior colliculus, is a sensorial nucleus with
unique characteristics.

In the mesencephalic nucleus of the trigeminus, neurons associated with extraocular
muscles are present along with the primary afferent neurons associated with the muscles
of the MM, tooth pulp and periodontal ligaments. From the mesencephalic nucleus of
the trigeminus, the neural pathways connect with the cerebellum, the reticular formation
and the medial, inferior, lateral and superior vestibular nuclei.

This cross-sectional study was carried out by observing 605 subjects. Analysis of
cross-sectional data usually consists of comparing the differences among the subjects,
as well as yielding incidence rates for any single disorder. These data can only describe
the incidence proportion of the contemporary presence of occlusal, orthoptic and postural
disorders.

In this epidemiological survey, we assessed that:

About 13% of the children showed a pathological gait and, among them, patients with
vertical anomalies of occlusion (deep bite or open bite) seemed to demonstrate a higher
prevalence (with a statistically significant difference of 2%) of a pathological gait;

About 5%–6% of the entire sample demonstrated dysmetric legs, which can explain only
50% of the cases with a pathological gait;

The vertical dimension of occlusion revealed a slight relationship with the proper
dominant eye, as deep bite patients showed a significantly lower tendency towards
a left dominant eye (p < 0.05). Therefore, more were likely to show a right dominant
eye. At the same time, deep bite subjects revealed a significantly lower frequency
of pathological convergence in their right eye (p < 0.05). Deep bite subjects had
the tendency to show more frequent CT exophoria at a significant level (p < 0.05),
while open bite patients showed a significantly lower percentage of CT esophoria.

Conclusions

In conclusion, postural, orthoptic and occlusal alterations may be clinically associated.
Clinical connections or concomitant frequencies can be found among them, often with
significant differences. From these data, it is not possible to state that there is
a direct causal connection among them, but we may suppose that a causal connection
may exist. Therefore, the treatment of such disorders requires the intervention of
several specialists and a multidisciplinary approach. It is very important that pediatricians
are aware of these possible clinical associations to direct young patients to the
appropriate specialists that may treat these various disorders. In addition, it can
be concluded that when a child is suffering from one of these disorders (postural,
occlusal or orthotic), it may be useful for them to undergo screening for other possibly
associated disorders.

Competing interests

For this study, there was no conflict of interest in: (1) the study design; (2) the
collection, analysis and interpretation of data; (3) the writing of the report; and
(4) the decision to submit the paper for publication.

Armando Silvestrini-Biavati wrote the first draft of the manuscript and no honorarium,
grant, or other form of payment was given to anyone to produce the manuscript.

Authors’ contributions

ASB and PSB conceived the study; MM, EDM, ASB and PSB recorded the data; ST analyzed
the data; ASB, MM, MS and PSB organized the manuscript and interpreted the results;
MS and AP followed the statistical evaluation and reviewed the text; MS and ASB coordinated
the work. All authors read and approved the final manuscript.

Acknowledgements

The authors would like to thank Dr. G. Pittaluga, Dr. L. Berta, Dr. G. Cavallero,
Dr. A. Ghidoni (School Medicine-District 1-Genova), who assisted with sample recruitment
and administrative school planning, and Dr. F. Aliotta (osteopathist), Dr. E. Artuso
(orthoptist) , Dr. V. Parodi for their important assistance and work during the clinical
examinations.